Identifying drivers of non-stationary climate-growth relationships of European beech.

The future performance of the widely abundant European beech (Fagus sylvatica L.) across its ecological amplitude is uncertain. Although beech is considered drought-sensitive and thus negatively affected by drought events, scientific evidence indicating increasing drought vulnerability under climate change on a cross-regional scale remains elusive. While evaluating changes in climate sensitivity of secondary growth offers a promising avenue, studies from productive, closed-canopy forests suffer from knowledge gaps, especially regarding the natural variability of climate sensitivity and how it relates to radial growth as an indicator of tree vitality. Since beech is sensitive to drought, we in this study use a drought index as a climate variable to account for the combined effects of temperature and water availability and explore how the drought sensitivity of secondary growth varies temporally in dependence on growth variability, growth trends, and climatic water availability across the species' ecological amplitude. Our results show that drought sensitivity is highly variable and non-stationary, though consistently higher at dry sites compared to moist sites. Increasing drought sensitivity can largely be explained by increasing climatic aridity, especially as it is exacerbated by climate change and trees' rank progression within forest communities, as (co-)dominant trees are more sensitive to extra-canopy climatic conditions than trees embedded in understories. However, during the driest periods of the 20th century, growth showed clear signs of being decoupled from climate. This may indicate fundamental changes in system behavior and be early-warning signals of decreasing drought tolerance. The multiple significant interaction terms in our model elucidate the complexity of European beech's drought sensitivity, which needs to be taken into consideration when assessing this species' response to climate change.

High preseason temperature variability drives convergence of xylem phenology in the Northern Hemisphere conifers.

Wood growth is key to understanding the feedback of forest ecosystems to the ongoing climate warming. An increase in spatial synchrony (i.e., coincident changes in distant populations) of spring phenology is one of the most prominent climate responses of forest trees. However, whether temperature variability contributes to an increase in the spatial synchrony of spring phenology and its underlying mechanisms remains largely unknown. Here, we analyzed an extensive dataset of xylem phenology observations of 20 conifer species from 75 sites over the Northern Hemisphere. Along the gradient of increase in temperature variability in the 75 sites, we observed a convergence in the onset of cell enlargement roughly toward the 5th of June, with a convergence in the onset of cell wall thickening toward the summer solstice. The increase in rainfall since the 5th of June is favorable for cell division and expansion, and as the most hours of sunlight are received around the summer solstice, it allows the optimization of carbon assimilation for cell wall thickening. Hence, the convergences can be considered as the result of matching xylem phenological activities to favorable conditions in regions with high temperature variability. Yet, forest trees relying on such consistent seasonal cues for xylem growth could constrain their ability to respond to climate warming, with consequences for the potential growing season length and, ultimately, forest productivity and survival in the future.

Temporal and spatial variability of phloem structure in Picea abies and Fagus sylvatica and its link to climate.

Using a unique 8-year data set (2010-2017) of phloem data, we studied the effect of temperature and precipitation on the phloem anatomy (conduit area, widths of ring, early and late phloem) and xylem-ring width in two coexisting temperate tree species, Picea abies and Fagus sylvatica, from three contrasting European temperate forest sites. Histometric analyses were performed on microcores taken from tree stems in autumn. We found high interannual variability and sensitivity of phloem anatomy and xylem-ring widths to precipitation and temperature; however, the responses were species- and site-specific. The contrasting response of xylem and phloem-ring widths of the same tree species to weather conditions was found at the two Slovenian sites generally well supplied with precipitation, while at the driest Czech site, the influence of weather factors on xylem and phloem ring widths was synchronised. Since widths of mean annual xylem and phloem increments were narrowest at the Czech site, this site is suggested to be most restrictive for the radial growth of both species. By influencing the seasonal patterns of xylem and phloem development, water availability appears to be the most important determinant of tissue- and species-specific responses to local weather conditions.

Evidence of Woodland Management at the Eneolithic Pile Dwellings (3700-2400 BCE) in the Ljubljansko Barje, Slovenia?

It is assumed that people practiced woodland management, i.e., coppicing and pollarding, in prehistory, but details are poorly known. This study aims for a better understanding of woodland exploitation through time in the wetland basin of the Ljubljansko barje, Slovenia, from 3700-2400 BCE (Before Common Era). To do so, uncarbonized, waterlogged wood from 16 Eneolithic pile dwellings situated in two geographical clusters that cover a time span of c. 1300 years were subjected to age/diameter analysis. It is the first time that age/diameter analysis has been applied to multiple sites from the same region. The investigated posts represent a wide range of taxa, but oak (Quercus sp.) and ash (Fraxinus sp.) represent 75% of the total, indicating selective use of wood for this purpose. Diameter selection of ash may have taken place as well. At both site clusters, the age/diameter data do not reveal any unequivocal evidence for woodland management. Only at the youngest sites do the data possibly show some gradually changing practices. The outcomes are discussed within the framework of recent discussions about woodland management in Europe.

A critical thermal transition driving spring phenology of Northern Hemisphere conifers.

Despite growing interest in predicting plant phenological shifts, advanced spring phenology by global climate change remains debated. Evidence documenting either small or large advancement of spring phenology to rising temperature over the spatio-temporal scales implies a potential existence of a thermal threshold in the responses of forests to global warming. We collected a unique data set of xylem cell-wall-thickening onset dates in 20 coniferous species covering a broad mean annual temperature (MAT) gradient (-3.05 to 22.9°C) across the Northern Hemisphere (latitudes 23°-66° N). Along the MAT gradient, we identified a threshold temperature (using segmented regression) of 4.9 ± 1.1°C, above which the response of xylem phenology to rising temperatures significantly decline. This threshold separates the Northern Hemisphere conifers into cold and warm thermal niches, with MAT and spring forcing being the primary drivers for the onset dates (estimated by linear and Bayesian mixed-effect models), respectively. The identified thermal threshold should be integrated into the Earth-System-Models for a better understanding of spring phenology in response to global warming and an improved prediction of global climate-carbon feedbacks.

Dendrochronological Dating and Provenancing of String Instruments.

Dendrochronology, the science of dating tree rings in the wood, defines in which calendar year a particular tree ring was formed. The method can be used to determine the age and authentication of wooden musical instruments. We present a protocol describing how to perform a dendrochronological analysis on stringed instruments and how to interpret the dating. The protocol describes the basic steps in the analysis of top plates, which are usually made of Norway spruce (Picea abies) or, more rarely, silver fir (Abies alba). First, the top plate is carefully inspected, and then the tree ring widths are measured directly on the instrument using high-resolution images. After completing the measurements, a tree ring sequence of the instrument is created, and, in the next step, dating is performed with a number of reference chronologies of the tree species from different geographical areas and instruments. The specialists who date the instruments also invest work in creating reference chronologies. The dendrochronological report provides the dating of an instrument as a calendar year (end date), indicating the year in which the last (most recent) tree ring on the top plate was formed when the tree was still alive. The end date represents the terminus post quem, the year after which the instrument was made or before which it could not have been made. To estimate the year of manufacture, one must consider the time required for wood drying and storing and the number of tree rings removed during wood processing. This protocol is intended to help those commissioning such an analysis to better understand how the analysis is performed and how to interpret the dendrochronological reports in terms of the age, origin, maker, and authenticity of the instrument.

Dominance of Fagus sylvatica in the Growing Stock and Its Relationship to Climate-An Analysis Using Modeled Stand-Level Climate Data.

In the future, climate change is expected to affect the spatial distribution of most tree species in Europe. The European beech (Fagus sylvatica), a drought-sensitive tree species, is currently distributed throughout Europe, where it is an ecologically and economically important species. In Slovenia, the European beech represents 33% of the growing stock, but such a proportion greatly varies across Europe. Whether such a variation is related to the climate environmental gradients or because of historical or management decisions is an as-yet unexplored question. For this study, we employed the Slovenian Forests Service inventory, where the proportion of beech in the forest stock has been monitored in 341,341 forest stands across the country. Modeled climate data from the SLOCLIM database, calculated for each of the stands, was also used to test the hypothesis that although beech forests have always been influenced by human activity, the dominance of beech trees in forest stands is at least partially dictated by the climate. The results showed the distribution of the main climate variables (annual precipitation, the share of summer and spring precipitation, and annual maximum and minimum temperatures) and how they affect the current dominance of beech trees at the stand level. Due to the large number and variability of forest stands studied, the results should be transferable to better understand and manage the climatic suitability and risks of Fagus sylvatica. The modeled data is publicly available in the web repository Zenodo.

Climate-change-driven growth decline of European beech forests.

The growth of past, present, and future forests was, is and will be affected by climate variability. This multifaceted relationship has been assessed in several regional studies, but spatially resolved, large-scale analyses are largely missing so far. Here we estimate recent changes in growth of 5800 beech trees (Fagus sylvatica L.) from 324 sites, representing the full geographic and climatic range of species. Future growth trends were predicted considering state-of-the-art climate scenarios. The validated models indicate growth declines across large region of the distribution in recent decades, and project severe future growth declines ranging from -20% to more than -50% by 2090, depending on the region and climate change scenario (i.e. CMIP6 SSP1-2.6 and SSP5-8.5). Forecasted forest productivity losses are most striking towards the southern distribution limit of Fagus sylvatica, in regions where persisting atmospheric high-pressure systems are expected to increase drought severity. The projected 21st century growth changes across Europe indicate serious ecological and economic consequences that require immediate forest adaptation.

Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers.

Wood formation consumes around 15% of the anthropogenic CO2 emissions per year and plays a critical role in long-term sequestration of carbon on Earth. However, the exogenous factors driving wood formation onset and the underlying cellular mechanisms are still poorly understood and quantified, and this hampers an effective assessment of terrestrial forest productivity and carbon budget under global warming. Here, we used an extensive collection of unique datasets of weekly xylem tissue formation (wood formation) from 21 coniferous species across the Northern Hemisphere (latitudes 23 to 67°N) to present a quantitative demonstration that the onset of wood formation in Northern Hemisphere conifers is primarily driven by photoperiod and mean annual temperature (MAT), and only secondarily by spring forcing, winter chilling, and moisture availability. Photoperiod interacts with MAT and plays the dominant role in regulating the onset of secondary meristem growth, contrary to its as-yet-unquantified role in affecting the springtime phenology of primary meristems. The unique relationships between exogenous factors and wood formation could help to predict how forest ecosystems respond and adapt to climate warming and could provide a better understanding of the feedback occurring between vegetation and climate that is mediated by phenology. Our study quantifies the role of major environmental drivers for incorporation into state-of-the-art Earth system models (ESMs), thereby providing an improved assessment of long-term and high-resolution observations of biogeochemical cycles across terrestrial biomes.

Low growth resilience to drought is related to future mortality risk in trees.

Severe droughts have the potential to reduce forest productivity and trigger tree mortality. Most trees face several drought events during their life and therefore resilience to dry conditions may be crucial to long-term survival. We assessed how growth resilience to severe droughts, including its components resistance and recovery, is related to the ability to survive future droughts by using a tree-ring database of surviving and now-dead trees from 118 sites (22 species, >3,500 trees). We found that, across the variety of regions and species sampled, trees that died during water shortages were less resilient to previous non-lethal droughts, relative to coexisting surviving trees of the same species. In angiosperms, drought-related mortality risk is associated with lower resistance (low capacity to reduce impact of the initial drought), while it is related to reduced recovery (low capacity to attain pre-drought growth rates) in gymnosperms. The different resilience strategies in these two taxonomic groups open new avenues to improve our understanding and prediction of drought-induced mortality.

Testing three climate datasets for dendroclimatological studies of oaks in the South Carpathians.

Three gridded datasets containing interpolated daily and monthly precipitation and temperature values over the past five decades were tested against four tree-ring chronologies of oak (Quercus robur and Q. petraea). The objective of this research was to investigate the climate-growth relationship and whether the Pearson's product-moment correlation coefficients differ significantly if mean monthly precipitation and temperature data from the different climate databases, CRU, E-OBS and ROCADA are used. To this end, we selected two representative oak ecosystems in the South Carpathians, Romania, and analysed earlywood, latewood and tree-ring widths. Climate time series trends for the South Carpathians coldest, warmest days and wettest days were assessed with datasets from E-OBS and ROCADA, which differed in the density of their meteorological station network and their interpolation methods. The observed climatic parameters showed changes towards wetter conditions after the mid-1980s. For 1961-2013, E-OBS underestimated the mean daily temperature and daily precipitation compared with ROCADA. The results showed that higher extreme temperatures from January-March affected earlywood growth. In the investigated study region, latewood formation seemed to be affected by water availability mainly in May. Periods of drought associated with higher temperatures have limiting effects on tree growth, but these events are captured in different ways by each climate database analysed. Similarly, the results showed the discrepancy among datasets for earlywood and climate relationships. The results emphasize the importance of proper selection of climate data for assessing climate-tree growth relationships. For future dendroclimatological and dendroecological studies of oak in Romania, we recommend the ROCADA database, while E-OBS is recommended if an up-to-date climate dataset is needed.

Chilling and forcing temperatures interact to predict the onset of wood formation in Northern Hemisphere conifers.

The phenology of wood formation is a critical process to consider for predicting how trees from the temperate and boreal zones may react to climate change. Compared to leaf phenology, however, the determinism of wood phenology is still poorly known. Here, we compared for the first time three alternative ecophysiological model classes (threshold models, heat-sum models and chilling-influenced heat-sum models) and an empirical model in their ability to predict the starting date of xylem cell enlargement in spring, for four major Northern Hemisphere conifers (Larix decidua, Pinus sylvestris, Picea abies and Picea mariana). We fitted models with Bayesian inference to wood phenological data collected for 220 site-years over Europe and Canada. The chilling-influenced heat-sum model received most support for all the four studied species, predicting validation data with a 7.7-day error, which is within one day of the observed data resolution. We conclude that both chilling and forcing temperatures determine the onset of wood formation in Northern Hemisphere conifers. Importantly, the chilling-influenced heat-sum model showed virtually no spatial bias whichever the species, despite the large environmental gradients considered. This suggests that the spring onset of wood formation is far less affected by local adaptation than by environmentally driven plasticity. In a context of climate change, we therefore expect rising winter-spring temperature to exert ambivalent effects on the spring onset of wood formation, tending to hasten it through the accumulation of forcing temperature, but imposing a higher forcing temperature requirement through the lower accumulation of chilling.

High-Throughput DNA sequencing of ancient wood.

Reconstructing the colonization and demographic dynamics that gave rise to extant forests is essential to forecasts of forest responses to environmental changes. Classical approaches to map how population of trees changed through space and time largely rely on pollen distribution patterns, with only a limited number of studies exploiting DNA molecules preserved in wooden tree archaeological and subfossil remains. Here, we advance such analyses by applying high-throughput (HTS) DNA sequencing to wood archaeological and subfossil material for the first time, using a comprehensive sample of 167 European white oak waterlogged remains spanning a large temporal (from 550 to 9,800 years) and geographical range across Europe. The successful characterization of the endogenous DNA and exogenous microbial DNA of 140 (~83%) samples helped the identification of environmental conditions favouring long-term DNA preservation in wood remains, and started to unveil the first trends in the DNA decay process in wood material. Additionally, the maternally inherited chloroplast haplotypes of 21 samples from three periods of forest human-induced use (Neolithic, Bronze Age and Middle Ages) were found to be consistent with those of modern populations growing in the same geographic areas. Our work paves the way for further studies aiming at using ancient DNA preserved in wood to reconstruct the micro-evolutionary response of trees to climate change and human forest management.

Precipitation is not limiting for xylem formation dynamics and vessel development in European beech from two temperate forest sites.

We investigated the dynamics of xylem differentiation processes and vessel characteristics in Fagus sylvatica L. to evaluate the plasticity of xylem structures under different environmental conditions. In 2008-10, analyses were performed on microcores collected weekly from two temperate sites: Menina planina (1200 m above sea level (a.s.l.)) and Panska reka (400 m a.s.l.). The duration between the onset and end of major cell differentiation steps and vessel characteristics (i.e., density, VD; mean diameter, MVD; mean area, MVA; and theoretic conductivity area, TCA) were analysed in the first and last quarters of the xylem rings, also in respect of local weather conditions (precipitation, temperature). Although the onset, duration and end of xylem formation phases differed between the two sites, the time spans between the successive wood formation phases were similar. Significant differences in MVD, MVA and TCA values were found between the first and last quarters of xylem increment, regardless of the site and year. Vessel density, on the other hand, depended on xylem-ring width and differed significantly between the sites, being about 30% higher at the high elevation site, in beech trees with 54% narrower xylem rings. Vessel density in the first quarter of the xylem ring showed a positive correlation with the onset of cell expansion, whereas a negative correlation of VD with the cessation of cell production was found in the last quarter of xylem increment. This may be explained by year-to-year differences in the timing of cambial reactivation and leaf development, which effect hormonal regulation of radial growth. No significant linkage between intra-annual weather conditions and conduit characteristics was found. It can thus be presumed that precipitation is not a limiting factor for xylem growth and cell differentiation in beech at the two temperate study sites and sites across Europe with similar weather conditions.

Early-Warning Signals of Individual Tree Mortality Based on Annual Radial Growth.

Tree mortality is a key driver of forest dynamics and its occurrence is projected to increase in the future due to climate change. Despite recent advances in our understanding of the physiological mechanisms leading to death, we still lack robust indicators of mortality risk that could be applied at the individual tree scale. Here, we build on a previous contribution exploring the differences in growth level between trees that died and survived a given mortality event to assess whether changes in temporal autocorrelation, variance, and synchrony in time-series of annual radial growth data can be used as early warning signals of mortality risk. Taking advantage of a unique global ring-width database of 3065 dead trees and 4389 living trees growing together at 198 sites (belonging to 36 gymnosperm and angiosperm species), we analyzed temporal changes in autocorrelation, variance, and synchrony before tree death (diachronic analysis), and also compared these metrics between trees that died and trees that survived a given mortality event (synchronic analysis). Changes in autocorrelation were a poor indicator of mortality risk. However, we found a gradual increase in inter-annual growth variability and a decrease in growth synchrony in the last ∼20 years before mortality of gymnosperms, irrespective of the cause of mortality. These changes could be associated with drought-induced alterations in carbon economy and allocation patterns. In angiosperms, we did not find any consistent changes in any metric. Such lack of any signal might be explained by the relatively high capacity of angiosperms to recover after a stress-induced growth decline. Our analysis provides a robust method for estimating early-warning signals of tree mortality based on annual growth data. In addition to the frequently reported decrease in growth rates, an increase in inter-annual growth variability and a decrease in growth synchrony may be powerful predictors of gymnosperm mortality risk, but not necessarily so for angiosperms.

Critical minimum temperature limits xylogenesis and maintains treelines on the southeastern Tibetan Plateau.

Physiological and ecological mechanisms that define treelines are still debated. It has been suggested that the absence of trees above the treeline is caused by low temperatures that limit growth. Thus, we hypothesized that there is a critical minimum temperature (CTmin) preventing xylogenesis at treeline. We tested this hypothesis by examining weekly xylogenesis across three and four growing seasons in two natural Smith fir (Abies georgei var. smithii) treeline sites on the southeastern Tibetan Plateau. Despite differences in the timing of cell differentiation among years, minimum air temperature was the dominant climatic variable associated with xylem growth; the critical minimum temperature (CTmin) for the onset and end of xylogenesis occurred at 0.7±0.4°C. A process-based modelling chronology of tree-ring formation using this CTmin was consistent with actual tree-ring data. This extremely low CTmin permits Smith fir growing at treeline to complete annual xylem production and maturation and provides both support and a mechanism for treeline formation.

A synthesis of radial growth patterns preceding tree mortality.

Tree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still limited. We compiled a new pan-continental tree-ring width database from sites where both dead and living trees were sampled (2970 dead and 4224 living trees from 190 sites, including 36 species), and compared early and recent growth rates between trees that died and those that survived a given mortality event. We observed a decrease in radial growth before death in ca. 84% of the mortality events. The extent and duration of these reductions were highly variable (1-100 years in 96% of events) due to the complex interactions among study species and the source(s) of mortality. Strong and long-lasting declines were found for gymnosperms, shade- and drought-tolerant species, and trees that died from competition. Angiosperms and trees that died due to biotic attacks (especially bark-beetles) typically showed relatively small and short-term growth reductions. Our analysis did not highlight any universal trade-off between early growth and tree longevity within a species, although this result may also reflect high variability in sampling design among sites. The intersite and interspecific variability in growth patterns before mortality provides valuable information on the nature of the mortality process, which is consistent with our understanding of the physiological mechanisms leading to mortality. Abrupt changes in growth immediately before death can be associated with generalized hydraulic failure and/or bark-beetle attack, while long-term decrease in growth may be associated with a gradual decline in hydraulic performance coupled with depletion in carbon reserves. Our results imply that growth-based mortality algorithms may be a powerful tool for predicting gymnosperm mortality induced by chronic stress, but not necessarily so for angiosperms and in case of intense drought or bark-beetle outbreaks.

Quantitative Wood Anatomy-Practical Guidelines.

Quantitative wood anatomy analyzes the variability of xylem anatomical features in trees, shrubs, and herbaceous species to address research questions related to plant functioning, growth, and environment. Among the more frequently considered anatomical features are lumen dimensions and wall thickness of conducting cells, fibers, and several ray properties. The structural properties of each xylem anatomical feature are mostly fixed once they are formed, and define to a large extent its functionality, including transport and storage of water, nutrients, sugars, and hormones, and providing mechanical support. The anatomical features can often be localized within an annual growth ring, which allows to establish intra-annual past and present structure-function relationships and its sensitivity to environmental variability. However, there are many methodological challenges to handle when aiming at producing (large) data sets of xylem anatomical data. Here we describe the different steps from wood sample collection to xylem anatomical data, provide guidance and identify pitfalls, and present different image-analysis tools for the quantification of anatomical features, in particular conducting cells. We show that each data production step from sample collection in the field, microslide preparation in the lab, image capturing through an optical microscope and image analysis with specific tools can readily introduce measurement errors between 5 and 30% and more, whereby the magnitude usually increases the smaller the anatomical features. Such measurement errors-if not avoided or corrected-may make it impossible to extract meaningful xylem anatomical data in light of the rather small range of variability in many anatomical features as observed, for example, within time series of individual plants. Following a rigid protocol and quality control as proposed in this paper is thus mandatory to use quantitative data of xylem anatomical features as a powerful source for many research topics.

Missing Rings in Pinus halepensis - The Missing Link to Relate the Tree-Ring Record to Extreme Climatic Events.

Climate predictions for the Mediterranean Basin include increased temperatures, decreased precipitation, and increased frequency of extreme climatic events (ECE). These conditions are associated with decreased tree growth and increased vulnerability to pests and diseases. The anatomy of tree rings responds to these environmental conditions. Quantitatively, the width of a tree ring is largely determined by the rate and duration of cell division by the vascular cambium. In the Mediterranean climate, this division may occur throughout almost the entire year. Alternatively, cell division may cease during relatively cool and dry winters, only to resume in the same calendar year with milder temperatures and increased availability of water. Under particularly adverse conditions, no xylem may be produced in parts of the stem, resulting in a missing ring (MR). A dendrochronological network of Pinus halepensis was used to determine the relationship of MR to ECE. The network consisted of 113 sites, 1,509 trees, 2,593 cores, and 225,428 tree rings throughout the distribution range of the species. A total of 4,150 MR were identified. Binomial logistic regression analysis determined that MR frequency increased with increased cambial age. Spatial analysis indicated that the geographic areas of south-eastern Spain and northern Algeria contained the greatest frequency of MR. Dendroclimatic regression analysis indicated a non-linear relationship of MR to total monthly precipitation and mean temperature. MR are strongly associated with the combination of monthly mean temperature from previous October till current February and total precipitation from previous September till current May. They are likely to occur with total precipitation lower than 50 mm and temperatures higher than 5°C. This conclusion is global and can be applied to every site across the distribution area. Rather than simply being a complication for dendrochronology, MR formation is a fundamental response of trees to adverse environmental conditions. The demonstrated relationship of MR formation to ECE across this dendrochronological network in the Mediterranean basin shows the potential of MR analysis to reconstruct the history of past climatic extremes and to predict future forest dynamics in a changing climate.